Humans are social beings. One of the
primordial functions of the brain is to enable
optimal interaction with others. The success of
social interaction resides in the capacity to
understand others in terms of motor actions
(intentionality), emotional perception, and a
mnemic and comparative cognitive integration
which separates the self from others (empathy,
altruism). In psychology, all these capacities
are referred to collectively as Theory of Mind
(TOM). It has long been known that yawning is
"contagious"; ethologists speak of behavioural
imitation and neurologists refer to echokinesis,
a term coined by JM. Charcot. How does such
echokinesis turn yawning into a form of
non-verbal social communication related to TOM
and empathy?

The discovery of mirror neurons by Rizzolatti
and Gallese (1) offers a neurophysiological
explanation for TOM. In most vertebrates,
developing the capacity to explore the
environment, making decisions (especially in a
life-or-death response to a predator) and
general preparation for action involve the
activation of these mirror neurons, along with
motor neurons, in cortical motor areas. Mirror
neurons are activated when the movements and
actions of conspecifics are perceived,
indicating that intentional action and the
corresponding mental imagery share the same
neuronal structures. Hence, when a single pigeon
senses the approach of a pedestrian, the entire
flock automatically flies away, even though most
of the birds did not actually perceive the
danger. This cooperative motor automatism is a
result of adaptive responses selected by
evolution. It serves the group by providing
protection from predators. Echokinesis-induced
yawning does not correspond to this mechanism,
as indicated by its latent appearance and its
inconsistency. In fact, echokinesis only occurs
in situations of minimal mental stimulation
(public transport); during prolonged
intellectual effort, people are not susceptible
to this phenomenon. Using functional MRI (fMRI),
Schürmann
et al. (2) confirmed that during echokinetic
yawning, there is no activation of mirror
neurons in motor areas of the human brain (left
posterior inferior frontal cortex), whereas
these neurons are activated during observation
of other types of facial gestures (decoding of
intentionality). These ethological and
neurophysiological elements demonstrate that,
strictly speaking, echokinetic yawning is not
motor imitation.

Visual
recognition of one's environment involves
various neuronal circuits which distinguish
inanimate objects from living creatures (3).
Recognition of human faces involves specific
dedicated neurons in the temporal area.
The
inferior temporal region (IT) allows
immediate overall recognition of faces, both
their identity and their expression, apparently
through its own autonomous, non-hippocampal
memory (4). As for the superior temporal sulcus
(STS), it is specifically activated during
perception of eye and mouth movements, which
suggests its implication in the visual
perception of emotions, once again by the
activation of mirror neurons. These neurons mime
the expression perceived, helping the observer
to understand it. Schürmann et al. (2)
demonstrated that the STS is activated during
echokinetic yawning. This activation, automatic
and involuntarily, is transmitted to the left
peri-amygdala, the posterior cingulate cortex
and the precuneus. These structures are thought
to play a role in differentiating emotions
expressed by the human face and, especially, in
evaluating the sincerity of the sentiment
expressed.

Using
fMRI, Platek et al. (5) found a correlation
between personality traits and the activation of
neuronal circuits beyond the STS. « In
contrast to those that were unaffected by seeing
someone yawn, people who showed contagions
yawing identified their own faces faster, did
better at making inferences about mental states,
and exhibited fewer schizotypal personality
characteristics. These results suggest that
contagious yawning might be related to
selfawareness and empathic processing »(6).
Subjects considered empathetic, who were very
susceptible to echokinetic yawning, activated
the peri-amygdala but not the amygdala and the
cingulate cortex, whereas schizotypal subjects,
who were not susceptible to this type of
yawning, did activate the amygdala (fear ?).
Neurophysiological
studies of empathy (7) show similar zones of
activation (STS, insula, amygdala, cingulate
cortex). These data imply that contagious
yawning may reside in brain substrates which
have been implicated in self-recognition and
mental state attribution, namely the right
prefrontal cortex.

During echokinetic yawning, frontal lobes
show no inhibitor activity. Therefore, it
appears that while the understanding of
intentionality (motor mirror neurons) and the
sharing of the emotions (mirror neurons in the
insula, amygdala and right parietal cortex)
require a common action-perception neuronal
activation and, simultaneously, frontal
inhibition (orbitofrontal activation) to prevent
motor exteriorisation, echokinetic yawning
cannot be inhibited involuntarily due to the
potentially absence of frontal inhibiting
relays. In contrast, the right temporoparietal
activation makes it possible to differentiate
between the self and others, and thus identify
on a conscious level that another person's yawn
has acted as a trigger (8).
Yawning could thus illustrate the simulation
theory of mind. In 2008, F. Nahab
et al. write "specifically associated with the
viewing of the contagious yawn was an area of
activation in the ventromedial prefrontal
cortex. These findings suggest a role for the
prefrontal cortex in the processing of
contagious yawning, while demonstrating a unique
automaticity in the processing of contagious
motor programs which take place independently of
mirror neuron networks".

Whereas yawning is universal amongst
vertebrates, it appears that only primates are
capable of echokinetic yawning. Anderson
(9) reported that chimpanzees yawn while
watching a video of their conspecifics yawning,
but not while watching other facial expressions.
Chimpanzees thus appear to be susceptible to
echokinetic yawning in the same way humans are.
Although the existence of a TOM
in chimpanzees remains controversial (10),
the observation of echokinetic yawning in this
species argues in favour of different levels of
TOM, which are perhaps secondary to the
different evolutionary paths of cognitive
development in hominids. Human psychiatric
pathology also dissects TOM in a similar way
(11). In 2008, A. Senju
et al. conduct the first study which seems to
demonstrate that human yawns are possibly
contagious to domestic dogs (Canis familiaris).
If the dogs' capacity for contagious yawning has
evolved with the capacity for reading human
communicative signals, it is possible that dogs
are more sensitive to human yawns than dogs'
yawns.

A.
Senju et al. (14) showed video clips of
people either yawning or simply opening and
closing their mouths to 49 children who were 7
years or older, half of whom were autistic. The
yawning faces triggered more than twice as many
yawns in non-autistic children than in their
autistic counterparts. This study
suggest that contagious yawning is
impaired in autism spectrum disorders, which may
relate to their impairment in empathy

Anderson
(12) showed that children were only susceptible
to echokinesis-induced yawning during their
sixth year, i.e. after acquiring the ability to
reflect on what others are thinking and
attribute mental states accordingly. In other
words, one must possess a state of cognitive
maturity on a functional level to be susceptible
to echokinetic yawning. Consequently, there is a
phenomenological link between the capacity to
attribute mental states to others (TOM), which
is the basis for empathy, and what is commonly
referred to as contagious yawning. In addition
to the neuroanatomical hierarchy separating TOM
into sensorimotor, emotional and cognitive
levels, echokinetic yawning makes it possible to
disassociate TOM, via its ontogenesis and its
phylogenesis, into various developmental levels,
an approach which is reinforced by the
differential activation of specific neuronal
circuits (13).
This type of yawning may have conferred a
selective advantage by synchronising the level
of vigilance between the members of a social
group. It may also take part in a form of
involuntary instinctive empathy, which could be
qualified as rudimentary and probably appeared
late in the course of hominid evolution (in the
neomammalian brain proposed by P.
McLean).

F.
Giganti et al. : The contagious effect of
yawning was present in young subjects and
young-old subjects, whereas it seems to
disappear in old-old subjects.The parallel
changes of contagious yawning and ToM abilities
across the lifespan suggest that similar
mechanisms are involved in ToM abilities, like
in contagious sensitivity to yawning. Besides,
changes in the response to other's people yawns
during very old age could reflect ToM
difficulties, reported in old-old subjects,
mainly in the cognitive component of ToM.

I am glad to offer a very interesting paper,
submitted orally to a congress in 1974 and never
published, in respect to the later studies of
Provine,
Platek,
Schürmann,
Anderson
and others.

"Like eating, yawning is an everyday
phenomenon which can be both internally (i.e.,
due to weariness) and externally (e.g., seeing
someone else yawn) elicited. The present study
was designed

to demonstrate the existence of the
externally produced "social" yawn, and

to investigate the role of individual
differences in susceptibility to the contagious
yawn.

.............

These results suggest that the same factors
important in more traditional social influence
settings are also active in the contagion of
social behaviors like yawning. In particular,
individuals who conform in an Asch
paradigm, who are identifiable by the Barron
test (Barron, 1953), appear to also be the
individuals most susceptible to contagious
yawning. One may speculate further as to
parallels between yawning and the influence
process; for example, credibility of the model
yawner could affect degree of contagion."